Cryptic Diversity of Japanese Diaphanosoma (Crustacea: Cladocera)

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Cryptic diversity of Japanese Diaphanosoma (Crustacea: Cladocera) revealed by morphological and molecular assessments Csilla Lakatos,1,2 Jotaro Urabe,1 Wataru Makino1* 1 Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan 2 Department of Ecology, University of Debrecen, Debrecen, Hungary * Corresponding author: [email protected]

Received 13 March 2015; accepted 11 June 2015; published DD Month 2015

Abstract

We found 5 distinct species of Diaphanosoma from a variety of lakes in Japan according to morphological examination and genetic analyses with the DNA sequences of mitochondrial 16S ribosomal RNA and cytochrome c oxidase subunit I genes (mtCOI). Previously, D. brachyurum was thought to occur at temperate regions including Japan; however, we did not find D. brachyurum in Japan. Instead, we found D. cf. amurensis, which inhabited mainly natural habitats of high altitude and latitude, and D. cf. dubium, D. cf. orientalis, and D. cf. macrophthalma, which occurred in a variety of habitats from large natural lakes to small artificial ponds at low altitude. We also found another species from only one pond that possessed mtCOI sequences that matched almost completely with those from North American specimens and thus was probably nonindigenous Diaphanosoma. Concordance between the results of morphological identifications and genetic analyses showed that the DNA barcodes established in this study are useful to identify Diaphano- soma species in Japan and adjacent areas.

Key words: Diaphanosoma, distribution, DNA barcode, mitochondrial cytochrome c oxydase subunit I (mtCOI) gene, mitochondrial 16S ribosomal RNA gene (mt16S)

Introduction distributed cladocerans such as Holopedium gibberum (Rowe et al. 2007), Leptodora kindtii (Korovchinsky The genus Diaphanosoma is distributed world-wide, 2009, Xu et al. 2011), Chydorus sphaericus (Belyaeva except in Antarctica and New Zealand (Korovchinsky and Taylor 2009), and Polyphemus pediculus (Xu et al. 1992). In Japan, previous studies reported the occurrence 2009) has been rejected because each of these “species” of D. brachyurum in a variety of lakes and ponds, is assigned to more than one species. including pristine pools in high mountain moors (e.g., Recently, a thorough revision of Diaphanosoma based Taira 1989, 2000), large lakes of low altitude (e.g., on external morphology has restricted the occurrence of Kikuchi 1937, Murayama and Saisho 1967, Hanazato and D. brachyurum sensu stricto to the area from Europe to Yasuno 1987, Yoshida et al. 2001), and artificial Siberia and Central Asia (Korovchinsky 1992). Since reservoirs (Higuti 1960, Mizuno and Tetsukawa 1963, then, several Diaphanosoma species were recorded for the Watanabe 1965). This prevalence of D. brachyurum in first time in Japan, including D. dubium and D. orghidani Japan was largely due to using the European species (Korovchinsky 2000a, 2000b) and D. macrophthalma name under the belief that most zooplankton species are (Tanaka et al. 2004). In addition, 2 new species, D. cosmopolitan. After the 1970s, however, cladoceran orientalis (Korovchinsky 1986) and D. kizakiensis (Ko- taxonomy began to improve, with more detailed morpho- rovchinsky 2013), have been described based on logical descriptions and consideration of genetic data specimens collected in Japan. Korovchinsky (2013) has (Frey 1982, 1987, Korovchinsky 1997). As a result of also stated that Diaphanosoma amurensis is present and detailed studies, the cosmopolitanism in broadly D. excisum might be present in Japan.

DOI: 10.5268/IW-5.3.847 Inland Waters (2015) 5, pp. © International Society of Limnology 2015 2 Lakatos C, Urabe J, Makino W.

Although our understanding of the species diversity of S2) because these characters are useful for distinguishing Japanese Diaphanosoma has improved, as explained Diaphanosoma species recorded in Japan (Korovchinsky, above, little is known about ecological characteristics 1992, 2000b, 2013, Korovchinsky and Mirabdullaev such as the spatial distribution of these species within the 1995, Korovchinsky and Sheveleva, 2009). Note, Japanese islands. To clarify these ecological characteris- however, that for each of the above-mentioned Diaphano- tics, precise identification of Diaphanosoma at the species soma species, we did not examine specimens collected level is essential; however, the morphological diagnostic from the type localities outside of Japan (e.g., Uzbekistan characters of Diaphanosoma species are rather subtle and for D. macrophthalma). In the case of D. orientalis, unfor- minute, which may cause misunderstanding of the tunately, its type locality was not included in our sampling ecological characteristics of each species through misi- sites. In the present study, therefore, we appended a “cf.” dentification. In such situations, identification with the aid when naming Diaphanosoma specimens to avoid potential of DNA barcoding is known to be effective (Hebert et al. confusion with the naming of these species in the future. 2003, Costa et al. 2007, Rowe et al. 2007, Huemer et al. In genetic analyses, the 16S ribosomal RNA gene 2014). To date, however, there have been few genetic (mt16S) was sequenced for 2 individuals of each Diapha- analyses of Diaphanosoma species (Müller and Seitz nosoma species identified in each lake or pond. Their 1995, Elías-Gutiérrez et al. 2008, Briski et al. 2011, Young DNA was extracted with QuickExtract according to the et al. 2012, Prosser et al. 2013). manufacturer’s protocol. We then used the mt16S The objective of this study was to clarify the distribu- universal primers developed by Sarri et al. (2014) and suc- tion patterns of Diaphansoma species in Japan. Specifi- cessfully amplified a ~200 bp fragment for all individuals cally, we examined whether different Diaphansoma examined. The polymerase chain reaction (PCR) species occur in different types of lakes and ponds. For conditions consisted of 85 s of initial denaturation at 95 this purpose, we first morphologically identified Diapha- °C, followed by 35 cycles of 35 s at 95 °C, 1 min at 48 °C, nosoma collected in a variety of lakes and ponds across and 30 s at 72 °C, and a final extension of 5 min at 72 °C. Japan. Then, by developing a Diaphanosoma DNA After cleaning the PCR products with an ExoSap IT kit, sequence library, we examined the feasibility of morpho- we conducted cycle-sequencing with a BigDye Terminator logical identification of Diaphanosma species. We also sequencing kit. Sequencing was then executed from both checked whether any Diaphanosoma species should be directions with an ABI PRISM 3100-Avant Genetic treated as a complex of cryptic species. Finally, we used Analyzer (Applied Biosystems). Obtained sequences all the above data to compare the spatial distribution of (164–168 bp) were submitted to the DNA Data Bank of different Diaphanosoma species in Japan. Japan (DDBJ) under the Accession numbers LC059999 – LC060040. We edited the sequences with FINCH TV and Methods aligned them with CLUSTAL X (Thompson et al. 1997). The phylogeny of mt16S sequences was illustrated using a The present study used sets of ethanol-fixed Japanese neighbor-joining (NJ) tree, which was constructed in freshwater zooplankton samples (see Makino and Tanabe MEGA 6.06 (Tamura et al. 2013) applying Kimura 2 2009, Makino et al. 2010, 2013, Urabe et al. 2011 ) parameter (K2P) pairwise genetic distance, pairwise gap collected between 2003 and 2014. Samples from 316 deletions, and 1000 bootstrap replications. lakes and ponds collected between June and November in Because some studies have deposited partial sequences each year were examined. We found that Diaphanosoma of the mitochondrial cytochrome c oxidase subunit I was present in 137 of the 316 lakes and ponds; however, (mtCOI) gene of Diaphanosma in searchable genetic the condition of Diaphanosoma specimens was databases (Elías-Gutiérrez et al. 2008, Briski et al. 2011, suboptimal in 41 of these cases, and these were excluded Young et al. 2012, Prosser et al. 2013), we also examined from the analysis. Thus we analyzed Diaphanosoma the sequence of this gene region for several specimens individuals collected in 96 total lakes and ponds (see Sup- (Supplemental Table S1) to systematically compare plemental Table S1). Diaphanosma occurring in Japan with those in other We examined 2–4 adult females from each sampling regions. The mtCOI was amplified using a primer set of site by morphology. For the morphological identification LCO1490 and HCO2188 (Folmer et al. 1994) according of Diaphanosoma individuals, we inspected the head to the protocol in Makino and Tanabe (2009). The PCR shape, the relative length of the swimming antennae, the products were cleaned and sequenced as explained above, presence or absence of inner spines near the dorsal and obtained sequences (658 bp) were submitted to DDBJ junction of both valves of the carapace, and the patterns of under the Accession numbers LC060041–LC060059. We denticles and a thin setule along the posterior and postero- then aligned the obtained mtCOI sequences with those of ventral margins of the carapace (see Supplemental Table Diaphanosoma outside of Japan deposited in the genetic

© International Society of Limnology 2015 DOI: 10.5268/IW-5.3.847 Cryptic diversity of Japanese Diaphanosoma 3 databases. The phylogeny of aligned sequences (529 bp) D. cf. dubium was divided further into 2 sub-clusters, was depicted in an NJ tree with the aid of MEGA, using northern and southern lineages. On average, the interspe- the K2P pairwise genetic distance and 1000 bootstrap rep- cific sequence differentiations (15.5–28.6%) were larger lications. The sequence obtained from Holopedium than the intraspecific sequence differentiations (0.6–4.3%; gibberum, which was collected in a pool of Ukishima Table 1). In the cluster of D. cf. amurensis, the haplotype moor (DDBJ Accession number LC060060, this study), YBE16S01 was separated from the rest of the haplotypes. was used as an outgroup. Here again, however, the maximal sequence differentiation among the haplotypes within this cluster was 9.3%, Results smaller than the interspecific differentiations. The mtCOI phylogeny also distinguished the 5 Diaph- Using the diagnostic morphological characters described anosoma species (Fig. 2). The interspecific sequence dif- by Korovchinsky and colleagues for Diaphanosoma ferentiations ranged 19.9–25.6% (Table 2), which were at species in Japan (Supplemental Table S2), we identified 4 the typical degree of interspecific differentiation in Diaphanosoma species from Japanese lakes and ponds: D. crustaceans according to the DNA barcoding studies (e.g., cf. orientalis, D. cf. dubium, D. cf. macrophthalma, and D. Costa et al. 2007). Comparison of mtCOI haplotypes cf. amurensis. In addition to these species, we found one found in this study with those deposited in the databases more species that could not be identified according to the showed that the haplotypes of the D. cf. dubium southern morphological characters shown in Supplemental Table lineage were nearly identical to the haplotype from S2. We described this as Diaphanosoma sp. 1 in this study. Taiwanese “D. dubium” (Young et al. 2012). The In accord with the morphological observations, genetic haplotypes of Japanese D. cf. macrophthalma were similar examination with mt16S sequences separated the Diapha- to those observed in Korea as “Diaphanosoma sp.” nosoma specimens into 5 genetic clusters (Fig. 1). Among (Prosser et al. 2013). The haplotypes of our Diaphano- these, the cluster of D. cf. orientalis had 5 haplotypes, D. soma sp. 1 were nearly identical to those observed in cf. dubium had 10 haplotypes, and D. cf. macrophthalma North American specimens described as “D. brachyurum” had 11 haplotypes. The cluster of D. cf. amurensis had 14 (Briski et al. 2011) or “Diaphanosoma sp. 2” (Elías-Gutié- haplotypes, and D. sp. 1 had 2 haplotypes. The cluster of rrez et al. 2008).

Table 1. Average intraspecific and interspecific sequence differentiations for Diaphanosoma species examined in the present study based on the mt16S gene. Numbers in parentheses denote minimal and maximal sequence differentiations. Numbers of haplotypes were 14, 10, 5, 11, and 2 for D. cf. amurensis, D. cf. dubium, D. cf. orientalis, D. cf. macrophthalma, and D. sp. 1, respectively.

Species name Species name D. cf. amurensis D. cf. dubium D. cf. orientalis D. cf. macrophthalma D. sp. 1 D. cf. amurensis 4.3 (0.6–9.3) D. cf. dubium 28.6 (22.0–33.1) 3.2 (0.6–6.3) D. cf. orientalis 26.6 (21.9–31.7) 15.5 (12.4–20.3) 1.8 (0.6–3.1) D. cf. macrophthalma 24.5 (20.3–28.2) 21.1 (17.8–21.1) 19.4 (17.2–22.0) 2.7 (0.6–5.1) D. sp. 1 16.9 (13.4–18.7) 27.8 (24.5–30.9) 25.6 (23.8–27.3) 23.0 (18.7–26.2) 0.6 (0.6–0.6)

Table 2. Average intraspecies and interspecific sequence differentiations forDiaphanosoma species examined in the present study based on the mtCOI gene. Numbers in parentheses denote minimal and maximal sequence differentiations. Numbers of haplotypes were 5, 5, 3, 4, and 2 for D. cf. amurensis, D. cf. dubium, D. cf. orientalis, D. cf. macrophthalma, and D. sp. 1, respectively. Species name Species name D. cf. amurensis D. cf. dubium D. cf. orientalis D. cf. macrophthalma D. sp. 1 D. cf. amurensis 3.1 (0.2–3.1) D. cf. dubium 24.3 (22.7–26.0) 5.0 (0.2–7.9) D. cf. orientalis 21.9 (20.4–23.7) 25.5 (24.3–26.5) 0.7 (0.6–0.8) D. cf. macrophthalma 21.3 (20.7–21.9) 24.6 (23.5–25.2) 22.8 (22.5–23.3) 1.7 (0.2–2.6) D. sp. 1 19.9 (18.6–22.0) 21.6 (21.2–22.2) 24.9 (24.7–25.1) 25.5 (25.0–26.1) 0.9 (0.9–0.9)

DOI: 10.5268/IW-5.3.847 Inland Waters (2015) 5, pp. 4 Lakatos C, Urabe J, Makino W.

Fig 1. Neighbor-joining phylogram of the examined Diaphanosoma species based on partial sequences of the mt16S gene (~170 bp). The numbers on nodes indicate bootstrap percentages (shown when >50%). The name of Diaphanosoma sp. 1 in the present study is modified to Diaphanosoma sp. IW-2015-1 in the DNA Data Bank of Japan.

Fig 2. Neighbor-joining phylogram of Diaphanosoma based on mtCOI (529 bp), using the Kimura 2-parameter model for nucleotide substitu- tions. Sequences obtained in the present study are shown in bold. Note that the name of Diaphanosoma sp. 1 in the present study is modified to Diaphanosoma sp. IW-2015-1 in the DNA Data Bank of Japan. Sequences obtained from the genetic databases are labeled with their Accession numbers. The names of Diaphanosoma with quotation marks are those used in the genetic databases. The numbers above major nodes indicate bootstrap percentages (shown when >50%).

DOI: 10.5268/IW-5.3.847 Inland Waters (2015) 5, pp. 6 Lakatos C, Urabe J, Makino W.

D. cf. dubium was most frequently found and was amurensis occurred in 16 lakes and ponds and was distributed throughout all sampled regions of Japan except distributed from Hokkaido Island to the middle of Honshu Hokkaido Island (Fig. 3). The northern lineage of this Island. D. cf. orientalis was found only in 10 lakes and species occurred in 37 lakes and ponds while the southern ponds on Honshu Island, and Diaphanosoma sp. 1 lineage was found in 20 lakes and ponds (Table 3); 5 of occurred only in Nakanoike pond in Hyogo Prefecture. these sites contained both lineages. D. cf. macrophthalma Generally, only one Diaphanosoma species appeared also appeared in 26 lakes and ponds across Japan from per habitat (i.e., per lake, pond, or reservoir); however, in Hokkaido Island to Kyushu Island. The other species were 9 habitats we simultaneously found 2 Diaphanosoma found in limited geographical ranges. Thus D. cf. species: both D. cf. dubium and D. cf. orientalis were

Fig 3. Geographical distributions of Diaphanosoma species in Japan.

Table 3. Surface areas of lakes and ponds where each of the Diaphanosoma species occurred.

Surface area (ha) No. of lakes ≤0.1 0.1–1 1–10 10–100 100– 1000– 10 000– inhabited 1000 10 000 100 000 D. cf. amurensis 16 9 5 1 1 0 0 0 D. cf. dubium northern lineage 37 1 11 20 3 1 1 0 D. cf. dubium southern lineage 20 0 6 11 0 1 1 1 D. cf. orientalis 10 0 0 5 0 2 2 1 D. cf. macrophthalma 26 0 13 9 3 0 1 0 D. sp. 1 1 1 0 0 0 0 0 0 collected in 5 of the 9 habitats, and D. cf. dubium and D. cf. macrophthalma in the remaining 4 habitats (Supple- mental Table S1). These habitats included various types of waterbodies, from large lakes such as Lake Biwa to small artificial irrigation ponds. Although there were no common features in the habitats where 2 Diaphanosma species occurred, different species tended to occur in different types of waterbodies. For example, D. cf. amurensis inhabited lakes and ponds of high altitude and latitude (Fig. 4) and was often found in pools of mountain moors such as those in Ozegahara and Mt. Naeba (Table 3, Sup- plemental Table S2). The other Diaphanosoma species were not found in such pristine environments, but rather occurred mostly in waterbodies at <1000 m a.s.l, including both small artificial reservoirs and large natural lakes.

Discussion

According to morphological examination, we found 5 Diaphanosoma species, D. cf. orientalis, D. cf. dubium, D. cf. macrophthalma, D. cf. amurensis, and Diaphano- soma sp. 1, in various lakes and ponds across Japan. Genetic analysis showed that the variations in DNA sequences among these species were larger than those within each of these species, and that the degrees of interspecific sequence variations in mtCOI were in the range of Fig 4. The relationship between latitudes (°N) and altitudes (m) of typical values found in crustaceans (Costa et al. 2007); lakes and ponds where each of the Diaphanosoma species was thus, interspecific genetic differentiations in the present found. The symbol labeled with an arrow denotes Lake Suwa, where study seem to reflect species boundaries. These results the D. cf. dubium southern lineage and D. cf. orientalis were indicate that the morphological characters of Diaphano- detected. soma described by previous studies (e.g., Korovchinsky 1992, 2000b, 2013, Korovchinsky and Mirabdullaev For the last decade, the DNA sequence of the mtCOI 1995, Korovchinsky and Sheveleva 2009) are useful gene has been established as the standard genetic barcode diagnostic keys in species identification of this genus in for species delimitation (Hebert et al. 2003, Huemer et al. Japan. The concordance between morphological and 2014). Compared with the mtCOI barcodes, which are genetic analyses also showed that genetic information usually >600 bp, the mt16S sequences used in the present such as the DNA sequences used in this study is useful in study were only ~170 bp. Nonetheless, our study success- species identification of Diaphanosoma, especially for fully distinguished Diaphanosoma species by using the nontaxonomic experts who are not familiar with the short mt16S sequences. It is not clear whether these short biology and morphology of cladocerans. fragments of the mt16S gene would be functional in terms

DOI: 10.5268/IW-5.3.847 Inland Waters (2015) 5, pp. 8 Lakatos C, Urabe J, Makino W. of delimiting Diaphanosoma species in other geographical to unproductive environments with relatively lower areas as well. In general, however, it is advantageous to temperature. Note that D. cf. dubium in Japan was use short DNA fragments for the delimitation of species composed of 2 genetically distinct groups, northern and when possible because the next-generation sequencing southern lineages. According to the mtCOI sequences, technology for analyzing numerically large samples is individuals of the D. cf. dubium southern lineage were currently limited to short DNA fragments. Therefore, genetically close to those described as “D. dubium” in when Diaphanosoma species are examined genetically in Taiwan (Young et al. 2012), suggesting that at least the other geographical areas, we recommend that both the southern lineage of D. cf. dubium has evolved to adapt to mt16S mini-barcode of Sarri et al. (2014) and the standard warm waterbodies. mtCOI barcode be examined. Among Diaphanosma examined in this study, Previously, D. brachyurum was recorded in various individuals detected in Nakanoike pond were not waterbodies in Japan, from pristine pools in high-moun- identified by the morphological diagnostic characters. tain moors (e.g., Taira 1989, 2000) to large lakes and These individuals, named Diaphanosoma sp. 1, were artificial reservoirs at low altitude (Kikuchi 1937, genetically differentiated from the 4 other Diaphano- Hanazato and Yasuno 1987, Higuti 1960, Mizuno and soma species found in this study according to the DNA Tetsukawa 1963, Watanabe 1965, Murayama and Saisho sequences of their mtCOI and mt16S genes; however, the 1967, Yoshida et al. 2001). It now seems these records mtCOI sequence of Diaphanosoma sp. 1 was similar to were incorrect, however, simply due to the dearth of those of North American Diaphanosoma, called “D. taxonomic knowledge on Diaphanosoma. According to brachyurum” (Briski et al. 2011) and “Diaphanosoma sp. Korovchinsky (1992), the distribution of D. brachyurum 2” (Elías-Gutiérrez et al. 2008). The rare occurrence in sensu stricto is restricted from Europe to Siberia and Japan and the close similarity in the mtCOI barcode with Central Asia, and we did not find D. brachyurum sensu North American specimens collectively suggest that Di- stricto in Japan, even though we included various types of aphanosoma sp. 1 in Nakanoike pond is a nonindigenous waterbodies across Japan. In addition to the species found species in Japan. In recent years, the invasions of exotic in our survey, Korovchinsky (2013) listed D. orghidani, zooplankton species have been reported. For example, D. kizakiensis, and D. excisum as Diaphanosma species Daphnia pulicaria, which was not originally distributed inhabiting Japan; however, we could not find these in Japan but genetically close to the individuals of North species, which are presumably rare zooplankter species America, appeared suddenly in Lake Biwa (Urabe et al. limited both spatially and seasonally. 2003). Some lineages or clones of Daphnia galeata and In this study, D. cf. dubium was found most frequently, Daphnia pulex were also thought to be artificially followed by D. cf. macrophthalma. These species introduced into Japan from North America (Ishida and occurred in a variety of habitats across Japan, ranging Taylor 2007, So et al. 2015). Diaphanosoma sp. 1 may from large natural lakes to small artificial ponds at lower have invaded from North America in recent years as altitude. D. cf. orientalis also appeared in lakes and ponds well. at low altitude on Honshu Island, although the frequency of occurrence was limited; thus, the geographical distribu- Acknowledgements tion patterns of these species were highly overlapped. In this study, however, only one Diaphanosoma species was We thank the editor and anonymous reviewers for generally found per habitat, although there were providing useful comments and references. This research exceptions in some habitats, suggesting that these 3 was financially supported by a scholarship of the Campus species may occupy a similar niche and thus be competi- Hungary Program to CL, and by grants from the Ministry tively exclusive. Further observations are needed to reach of the Environment, Japan (the Environment Research and a solid conclusion because the numbers of individuals Technology Development Fund, No. D-1002) and from examined per habitat are not sufficient in the present the Japan Society for the Promotion of Science (25291094, study. In contrast to these species, D. cf. amurensis 19207003) to JU and those (16770011, 19770010, appeared in natural habitats at higher altitude and latitude, 23570015, 15H02380 and 15K07211) to WM. including pristine pools of high mountain moors. D. amurensis is distributed in northeast regions of the Asian References continent, including Far East Russia (Korovchinsky and Sheveleva 2009). Together with this information on the Belyaeva M, Taylor DJ. 2009. 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